Trends in Ecology & Evolution

Review

Coloration in Mammals
Tim Caro1,2,* and Ricardo Mallarino3

Mammalian colors and color patterns are some of the most diverse and Highlights
conspicuous traits found in nature and have been widely studied from Mammalian external appearances are
genetic/developmental and evolutionary perspectives. In this review we first well known and their developmental
and adaptive significance are under ac-
discuss the proximate causes underlying variation in pigment type (i.e., color)
tive study.
and pigment distribution (i.e., color pattern) and highlight both processes as
having a distinct developmental basis. Then, using multiple examples, we dis- Pigment regulation and pigment pattern-
cuss ultimate factors that have driven the evolution of coloration differences ing determine how hair color develops.

in mammals, which include background matching, intra- and interspecific Mammalian hair and skin color can
signaling, and physiological influences. Throughout, we outline bridges change during an individual’s lifetime.
between developmental and functional investigatory approaches that help
broaden knowledge of mammals’ memorable external appearances, and we Most mammals have dichromatic vision
but some monkeys and apes are trichro-
point out areas for future interdisciplinary research. matic which may influence pelage color-
ation involved in signaling.

The Diversity of Mammalian Color Patterns Most mammals, both prey and preda-
Zebras became striped after ‘standing half in the shade and half out of it, and what with the tors, are assumed to match their back-
slippery-slidy shadows of the trees falling on them’ [1]. ground. Nonetheless, diverse and
anachronistic color patches are used in
interspecific signaling, such as the
Although children learn the striking colors of mammals from an early age, that (zebras Equus sp.) aposematism seen in black and white
are striped, leopards (Panthera pardus) are spotted, and giant pandas (Ailuropoda melanoleuca) mephitids and porcupines.
are black and white, they are still kept in the dark as to how and why these coloration patterns
Coloration has consequences for heat
arise, shielded from science through fairy stories. Yet, we now know an increasing amount management, and also for UV protec-
about the development and function of mammalian coloration. Here, we summarize genetic tion, most famously skin coloration in
and developmental mechanisms underlying these phenotypes. Second, we review the functions humans.
of mammalian external appearances, a group in which crypsis predominates but where signaling
We attempt to integrate developmental
(see Glossary) to conspecifics and to predators occasionally prevails. Finally, we suggest ways in and evolutionary approaches to explain
which these approaches can be consolidated. the origins of mammalian coloration.

Genetics of Hair Pigmentation: Historical Perspective

Beginning in the 18th century China and Japan, so-called mouse fanciers collected,
maintained, and bred together unusual color morphs of wild mice [2]; in doing so, these
amateur geneticists generated mouse strains with distinct color variation. Thus, pigmentation
phenotypes in mice, and later rats and guinea pigs, were readily available for study.
1
School of Biological Sciences,
Coat-color phenotypes were used as early as the 1900s to test several fundamental
University of Bristol, 24 Tyndall Avenue,
concepts in genetics – from Mendelian inheritance [3,4] to linkage [5], to demonstrations Bristol BS81TQ, UK
2
of epistasis and pleiotropy [6]. Center for Population Biology, 1 Shields
Avenue, University of California, Davis,
CA 95616, USA
Because of the utility of pigment phenotypes, a sizeable list of genetic loci with well character- 3
Department of Molecular Biology,
ized phenotypes has since accumulated. The first pigmentation gene to be cloned, tyrosinase- Princeton University, 119 Lewis Thomas
Laboratory, Washington Road,
related-protein-1 (Tyrp1), was initially thought to be the gene responsible for albinism, but was
Princeton, NJ 08544, USA
later mapped, cloned, sequenced and correctly attributed to the tyrosinase locus [7,8]. Since
then, more than 100 genes affecting pigmentation have been cloned in mice and it is likely
that many more remain to be identified [9] with ongoing chemical mutagenesis programs *Correspondence:
(Mouse Genome Database). tmcaro@ucdavis.edu (T. Caro).

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© 2019 Published by Elsevier Ltd.
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Pigmentation Regulation and Patterning Glossary

Color variation in mammals is primarily determined by two factors: (i) pigment regulation, altering Albinism: a genetic condition that
the type, density and/or distribution of pigments along individual hairs; or (ii) pigment patterning, reduces the amount of melanin formed
in the skin, hair, and/or eyes.
altering the spatial distribution of pigmentation across the body. Both of these processes can Dichromat: possesses two
have profound effects on overall appearance, but likely have a distinct genetic basis and are man- independent channels for conveying
ifested in different parts of the developmental pathway. color information, derived from the two
different types of cone cells in the eye.
Diurnality: being active during the day.
Pigment regulation: mammalian hair color results from a complex process involving the migration, Eumelanin: the other type of melanin
differentiation, and regulation of melanocytes, the pigment producing cells in the epidermis [10]. produced by melanocytes in mammals.
Melanocytes can produce two types of melanin pigment, eumelanin and pheomelanin, Eumelanin is largely responsible for
through a process that is primarily determined by the interaction between Agouti and α-melanocyte black/brown hair.
Introgression: transfer of genetic
stimulating hormone (MSH) with the melanocortin-1 receptor (Mc1r) [11]. When Agouti is not material between hybridizing species.
present, α-MSH will readily bind to Mc1r, causing intracellular cAMP to accumulate inside the Pelage: the fur, hair, or wool of a
cell. cAMP accumulation leads to the downstream activation of Tyr and the eventual production mammal.
Pheomelanin: one of the two types of
of eumelanin. When Agouti is present, it binds to Mc1r and causes a decrease in the production
melanin produced by melanocytes in
of intracellular cAMP, which eventually leads to downregulation of Tyr and causes melanocytes mammals. Pheomelanin is largely
to switch from the production of eumelanin to pheomelanin [11]. Genomic changes in Agouti/Mc1r responsible for red/yellow hair.
as well as in the genes involved in the downstream enzymatic reactions governing melanin Signals: are acts or structures
produced by signalers , which have
synthesis underlie natural variation in mammalian coats [12].
evolved for the purpose of conveying
information to recipients, such that the
Pigment patterning: in vertebrates, several mechanisms may contribute to regional variation in information elicits a response in
melanin type, density, and distribution. During embryogenesis, neural crest cells differentiate recipients resulting in fitness
consequences that, on average, are
into melanoblasts (precursors of melanocytes) that migrate ventrally along the body axis. Melano-
positive for both the signaler and
blasts typically enter the epidermis, where some remain (in certain species), while others localize recipient.
to the hair follicles and differentiate into melanocytes. Once mature, these melanocytes can pro- Trichromat: possesses three
duce pigment, which is then packaged into melanosomes and transferred to keratinocytes of de- independent channels for conveying
color information, derived from the three
veloping hair [13]. different types of cone cells in the eye.

Pigment patterns can be classified as random and nonrandom, based on developmental origin
and appearance [12]. Random patterns, such as those seen in some breeds of domestic animals,
arise from stochastic developmental events affecting melanocyte behavior. For example, the
white-spotting phenotype commonly present in cats and dogs is caused by a failure of melano-
cyte migration. In contrast, nonrandom patterns, such as periodic stripes and spots, arise from
spatially constrained developmental processes. Recent advances in genomics show how molec-
ular mechanisms shape natural variation in mammalian pigment patterns. Although Agouti plays a
central role in regulating melanocyte behavior during hair growth (see above), a different isoform of
Agouti is expressed during development and can directly influence melanocyte maturation. In
Peromyscus mice, differences in the position of the dorsal/ventral pigmentation boundary, seen
in two locally camouflaged populations, are explained by changes in the spatial expression do-
main of Agouti that occur during embryonic development [14]. This example illustrates how the
same gene, through the production of different isoforms, can influence pigmentation patterning
(ventral-specific expression during development) and pigment distribution within a single hair
(switch from eumelanin to phaeomelanin production). In African striped mice, Rhabdomys
pumilio, which have a coat comprised of dark and light longitudinal stripes (Figure 1A), the tran-
scription factor ALX3 is expressed at high levels in the light stripes where it acts to repress mela-
nocyte differentiation and pigment production [15]. Kaelin and coworkers [16] used a
combination of association and gene expression studies to show that periodic patterns (spots
and stripes) in felids are established in two stages: first, when skin is developing, the gene Taqpep
is involved in setting a prepattern that is later implemented during hair growth by the gene Edn3; a
secreted factor that is expressed at high levels in the black spots of cheetahs (Acinonyx jubatus),

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Trends in Ecology & Evolution

Figure 1. Selected Species of Mammals That Are Currently Being Used to Further Understanding of
Developmentala and Evolutionaryb Mechanisms Driving Coloration in Mammals. Top left: African striped grass
mouse Lemniscomys pumilioa; top right: snowshoe hare Lepus americanusa,b; middle left: oldfield mouse Peromyscus
polionotus a,b; middle right: Preuss’s guenon Cercopithecus preussib; bottom left: plains zebra Equus quaggab; bottom
right: melanistic gray squirrel Sciurus carolinensisa (photographs from WikiMedia).

where it promotes melanocyte differentiation and proliferation. These three examples demon-
strate how specific genes, by being expressed in a spatially restricted fashion, can act to establish
color differences along the body. Remarkably, spatially restricted gene expression patterns can
also be seen at much smaller scales, such as within a single hair follicle: in Dun horses, Equus
ferus, the transcription factor TBX3 is expressed only in the posterior half of hair follicles, resulting
in radially asymmetric deposition of pigment in hair follicles [17].

Introgression as a Source of Color Variation

Although differences in color between and within individuals can be generated via changes in
the coding sequence of genes or the regulatory region of genes controlling pigment synthesis or pig-
ment patterning, it is becoming more evident through the use of genomic and molecular approaches
that factors other than mutations, such as introgression, play a major role in promoting color varia-
tion in mammals. For instance, melanism in North American gray wolves, Canis lupus, is caused by a
mutation in the K locus, which encodes a β-defensin protein that acts as an alternative ligand for

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Mc1r. By analyzing the evolutionary history of the melanistic K locus, Anderson and colleagues [18]
were able to determine that this mutation, which has risen to high frequency and displays signatures
of positive selection, originated in domesticated dogs and was transferred to wolves through past
hybridization events. Thus, a mutation originally selected in a domesticated animal has provided favor-
able genetic diversity in a natural population. In another example, southern populations of snowshoe
hares, Lepus americanus, no longer moult from a brown to a white coat in winter, like their northern
counterparts (Figure 1B), but remain brown all year. As southern populations experience milder
winters with less snow, brown coats allow them to better blend in with the environment and avoid
predator attack. Using association mapping and population genetic analyses, Jones and colleagues
[19] showed that this variation maps to a regulatory region in the gene Agouti, and that the brown win-
ter coat allele was likely introgressed from black-tailed jackrabbits (Lepus californicus). Thus,
introgression has provided snowshoe hares a key source of genetic variation to adapt to rapidly
changing environments. In another recent study, McRobie and coworkers [20] found that melanism
in gray (Sciurus carolinensis) and fox squirrels (Sciurus niger) is caused by the same amino acid
change in Mc1r, and that this allele likely originated in fox squirrels and introgressed into gray squirrels.
Each example illustrates the importance of introgression as a continuous source of genetic variation
upon which natural selection can act.

Color Change in Mammals

Despite the fact that hair color is largely determined by the genotype of an individual, mammal
pelage color is not necessarily fixed throughout the lifetime. Some changes are age-related: cer-
tain suids, felids, and artiodactyls, for instance, are born with spotted or striped coats that be-
come uniform when offspring become mobile. In pigs and peccaries, variegated pelage is
associated with litter size perhaps because neonate interactions attract predator attention [21],
whereas in felids and artiodactyls young are sequestered in hidden locations. Some pinniped
and primate species are born with natal coats, which neonates soon lose. Although we know
that white seal pups match a snowy white arctic background, or are dark if born in caves or on
predator-free islands [22], the functions of black, white, orange, or gray neonate pelage in pri-
mates remain elusive but include attraction of allomothers and reduction of infanticide by
males. Hair color may also change in old age as in the silvery white of human hair. Second, a
few mammals change color seasonally, such as ermines (Mustela erminea) and snowshoe
hares, to match a white arctic background in winter, and later to match background soil in spring,
a cycle that is being disrupted by climate change [23].

Turning from crypsis to intraspecific signals, mammalian pelage color may vary according to
dominance, as in males from uni-male units turning dark blue–black in the greater kudu
(Tragelaphus strepsiceros) or ashen in mountain gorillas (Gorilla beringei). Finally, skin color can
change rapidly due to hormones and vasodilation, particularly in primates. For example, tumes-
cent red genitalia may advertise fertility and possibly ability to raise offspring to independence in
female baboons (Papio cynocephalus) [24], and may be used in mate choice in rhesus macaques
(Macaca mulatta) [25]. Male genital hue or facial luminance can signal dominance, as in vervet
monkeys (Chlorocebus pygerythrus) or mandrills (Mandrillus sphinx), respectively [26–28]. Even
more rapid signaling is possible: changing blood supply can alter facial coloration in response
to anger or stress. Blushing in humans may be such an example, although surprisingly little
work has been conducted since Charles Darwin devoted a chapter to it in his 1872 book, the
Expressions of Emotions in Man and Animals [29].

Color Vision
Knowledge of species’ and individuals’ differing spectral sensitivities might help us understand
the role that external color appearances play in interspecific and intraspecific signaling. Mammals

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were originally thought to be trichromats based on their reptilian ancestry but evolved to be
dichromats with maximal retinal sensitivities in short and medium wavelengths of the visual
spectrum when they became nocturnal, so a priori, they might be expected to be dowdy.
However, some primates and perhaps a few marsupial species secondarily became trichromats
coincident with the advent of diurnality [30]. The evolution of routine trichromacy (see below) in
African and Asian monkeys and apes [30] may have been driven by the benefits of picking out
orange and red ripe fruits and edible young leaves from a background of mature green leaves
[31–33] but the relationship between vision and foraging benefits is complex [34,35]. Reconstruc-
tions of the ancestral states under maximum parsimony indicate that trichromatic color vision
evolved at the ancestor to extant tarsiidae–platyrrhine–catarrhine species before the evolution
of red skin or pelage, suggesting that the presence of color vision may have been necessary
for the evolution of red external appearance in primates [36] but the association is not strong [37].

Among catarrhine primates, both sexes discern hues in the red–green range and along the an-
cestral blue–yellow color axis [38]. This routine trichromacy is enabled by two distinct opsin
genes on the X chromosome that code for mid-wavelength-sensitive (MWS, green) and long-
wavelength-sensitive (LWS, red) cone photopigments, and a third autosomal opsin gene coding
for short-wavelength-sensitive (SWS, blue) pigments. In contrast, certain lemurs and most pri-
mate species from the Americas possess polymorphic trichromacy due to allelic variation of a sin-
gle mid- to long-wavelength-sensitive opsin gene (M/LWS). In these polymorphic species, some
females and all males are red–green color blind, and only females that are M/ LWS heterozygotes
are capable of trichromatic vision [38–40]. Howler monkeys (Alouatta sp.), however, are an ex-
ception and have independently evolved routine trichromacy similar to catarrhines; interestingly,
they are heavily reliant on young red leaves [41].

Whether trichromatic species are more colorful than dichromats is little researched but at present
the association seems weak [37]. A related proposal with stronger support is that medium- and
long-wave cone maximum sensitivities for trichromats are optimized for discriminating variations
in blood oxygen saturation so that trichromacy may also be linked to primate facial and sexual
skin coloration as found in Asian and African groups [28,42].

Evolutionary Drivers: Crypsis

Rodents and bats, constituting approximately one quarter and one fifth of mammals respectively,
are often dull browns or grays probably to match their background to avoid detection. Research
on rodent hair color has a long history with early North American mammologists such as Sumner,
Benson, Dice, and Blossom describing coat color variation in US southwestern desert rodents
[43]. For example, they showed that in the rock pocket mouse (Chaetodipus intermedius), coat
color typically matches that of rubble on which the mice live; the dorsal pelage varies from a
light, sandy color for populations found on some granites to dark, nearly black for populations
found on basalt lava flows. These pelage hues, in some cases stemming from Mc1r mutations
[44], are likely selected for by owl predation [45,46] with patterns of migration across different
substrates driven by stronger selection against light morphs on a dark background than against
dark morphs on light background [47] (Figure 1C). Phenotype–environment matches also occur
on much larger geographic scales [48], while interspecific comparisons of other small mammalian
prey species similarly indicate pelage coloration matches different backgrounds [49]. Back-
ground matching is the form of protective coloration whose genetic basis is best understood.

Of course, it is not just prey that need to remain cryptic. Carnivores need to approach prey unno-
ticed; think of white polar bears (Ursus maritimus) approaching seals hauled out on ice. Other car-
nivores and perhaps pinniped and cetacean piscivores wear spotted, dappled, or uniform fur to

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approach their prey undetected; ocelots (Leopardus pardalis) and tigers (Panthera tigris) on land
[50], gray seals (Halichoerus grypus) [22], and Atlantic spotted dolphins (Stenella frontalis) [51] at
sea are all examples of what used to be called aggressive coloration in Victorian times.

Beyond background matching, many mammalian prey are countershaded (dark on top, lighter
underneath). This pattern is common in both terrestrial and aquatic animals although the under-
lying mechanisms are hotly debated and include crypsis, protection from UV light, and reducing
abrasion [52]. In some mammals, the dark to light boundary on the animal’s lateral surface pre-
cisely counteracts the shadow cast by the animal’s own body [53] perhaps rendering it 2D and
thus more difficult to detect than a 3D object. However, there must be other influences on dorsal
pigmentary darkening: the white ventrum of murids hugging the ground is unlikely to have evolved
for the same reasons as a gerenuk (Litocranius walleri) with its long legs. Other mechanisms of
remaining cryptic through disruptive coloration, masquerade or transparency have yet to be iden-
tified in mammals.

Evolutionary Drivers: Signaling

Many aspects of coloration in birds are driven by male–male competition and female choice but
these evolutionary drivers seem to have less force in mammals, except perhaps in African and
Asian primates where ornamental skin patches are more common [54] and in gibbon species
where males and females differ in pelage color. Sexual differentiation in fur color is also found in
a tiny handful of other species such as the male ribbon seal’s (Histriophoca fasciata) red inflatable
nostril, the mouflon’s (Ovis orientalis) blond beard, and various dark male bovids and pinnipeds
but has received minimal study [55]. The best worked example is the black manes of lions
(Panthera leo) that are attractive to females but intimidating to other males [56], a male ornament
kept in check by overheating.

Color patches are used in interspecific signaling; the most famous being aposematic coloration in
mustelids that advertises noxious anal secretions [57]. However, contrasting color patches can
be used to thwart predators in other ways. Black flank stripes of gazelles amplify pursuit deterrent
stotting behavior [58], and conspicuous ear tips of lagomorphs may deter pursuit [59]. Some
color regions such as white heads in cetaceans may function to drive fish into shoals for easier
capture [51]. Complex primate face colors may signal species’ identity so as to avoid hybridization
in sympatric primate congeners [60,61] (Figure 1D). It is challenging for researchers to explain the
absence of sexual dichromatism in mammals where mate choice is common, or the anachronistic
distribution of color patches used in signaling to other species [62].

Perhaps the take home message is that there is no single evolutionary cause of conspicuous pel-
age in mammals [63]. Black and white coats of zebras are not a form of warning coloration
(Figure 1E): instead a growing number of studies indicate that stripes thwart attack by disease-
carrying biting flies [64–66]. In giant pandas, comparative work indicates white fur blends in
with background snow, black legs with deep forest shade, but black eyes spots and ears help
in individual recognition and signal aggressive intent [67]. Blackbuck (Antilope cervicapra) are
sharply countershaded (black above, white below) to counteract dark shadow cast by the glaring
tropical sun [53], while the functional significance of black and white coats of colobus species,
Malayan tapirs (Tapirus indicus) and orcas (Orcinus orca) are still enigmatic but likely to differ
from each other.

Evolutionary Drivers: Physiology

From first principles, we assume that external coloration has inevitable consequences for heat
load; lighter coats reflect heat and are found in deserts, for instance. However, we still know little

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about the relative contributions that hair color, density, length, and structure contribute to temper- Outstanding Questions
ature regulation in mammals. Like several other groups, mammals are darker in the tropics Can developmental biologists take
(Gloger’s rule) but the melanin that produces darker color has other consequences including advantage of recent advances in
genomic and molecular approaches to
being relatively impervious to abrasion, antimicrobial benefits, preventing UV-caused mutagene-
study the mechanisms underlying
sis, and absorbing heat, so that the underlying mechanisms for Gloger’s rule may be multifaceted natural variation in mammalian pigment
[68,69]. In an important study, Hetem and coworkers [70] implanted thermodevices in three dif- patterns?
ferently colored springbok (Antidorcas marsupialis); a species that is normally light brown in color
Can we incorporate mechanistic
although black and white morphs exist. Daily maximum temperatures of the black morph were
studies of color/color pattern formation
significantly higher than normal or white morphs in spring due to absorbing more solar radiation. into a comparative phylogenetic
Daily minimum temperatures in the winter were significantly lower for the white than the black or context so that we can understand
normal morphs. Thus, stabilizing selection appears to act at different periods over the year. In win- whether convergent phenotypes have
arisen through similar molecular
ter, black morphs reduce energy expenditure but experience higher heat load in summer. White
mechanisms?
morphs live close to the energetic edge in winter. The normal springbok occupies a compromise
position which may explain why few black and white morphs are found. Oddly, the relationship What factors constrain the evolution
between hair color and thermoregulation is little explored in other mammals. of conspicuous skin coloration in
primates?

Turning to UV radiation protection, humans are polymorphic for skin color with people living at Why do some primates have
higher latitudes having lighter skin than those nearer the tropics where UV radiation is stronger. distinctive natal coat coloration?
The underlying principles are well established and often used as an example of evolutionary
Why does conspicuous coloration
trade-offs in teaching students about evolution. On the one hand, eumelanin prevents UV from evolve in mammals that are not
causing oxidative damage to DNA which can result in skin cancer. Additionally, it prevents vitamin aposematic?
B folate photolysis. Folic acid is an essential nutrient needed in nucleotides and hence DNA syn-
Why is sexual dichromatism so rare in
thesis, especially in maturing bone marrow and developing red blood cells. Exposure to excessive mammals?
amounts of UV leads to folate deficiency and this results in fetal abnormalities especially spina
bifida and anencephalitis where the neural tube fails to close properly in the developing embryo. What are the mechanisms underlying
Gloger’s rule in mammals?
On the other hand, UV promotes the synthesis of Vitamin D3 in the skin. Vitamin D has many pos-
itive effects including promoting bone formation and mineralization and reducing cardiovascular
disease, diabetes, multiple sclerosis, and inflammatory bowel disease. While there is sufficient
UV at lower latitudes for people to synthesize vitamin D, even with melanized skin, there is not
enough UV at higher latitudes so people must reduce melanin synthesis and consequently
have lighter skin. Humans living in intermediate latitudes (in the Mediterranean) with high annual
variance in UV show facultative tanning in which melanization starts slowly allowing vitamin D pro-
duction to occur in spring and winter, but prevention of vitamin B folate photolysis in hot summer
months [71,72].

In addition to the physiological impacts of differences in color described above, it is worth noting
that the physiology of an organism can have a large impact on color production, mediated by hor-
mones. For example, melatonin and prolactin play a key role in regulating seasonal moulting in
various animals: when days get shorter, specialized photosensitive ganglion cells in the eye retina
convey a signal that ultimately reaches the pineal gland, which controls secretion of melatonin.
Melatonin is produced at night at rates that are inversely proportional to day length. During the
winter, as days get shorter, higher levels of melatonin inhibit the production of prolactin, leading
to the production of white winter fur [73].

Concluding Remarks and Future Perspectives

At present, the study of mammalian coloration is divided into two camps – developmental and
evolutionary – that, with notable exceptions [14,74–76], interact infrequently (hence our attempt
here). Developmental biologists concentrate on cellular mechanisms and morphology, whereas
evolutionary ecologists focus on behavioral and ecological variables to explain macroevolutionary
patterns. Moreover, the former relies on model systems of a handful of species whereas the latter

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often focuses on many species in a clade. We see three ways to bridge this divide (see
Outstanding Questions). First, we need to test the ecological significance of phenotypes being
studied at the molecular level. Already experimental and observational studies show that different
selective backgrounds drive population gene frequencies [76]; that the relative strengths of selec-
tion on alleles that code for pelage background matching differ according to habitat [77]; and that
changing ecology can precede changes in genetic variation [78]. However, although we under-
stand that the terminal differentiation of ventral melanocytes is delayed in mice that are
countershaded as adults [14], we do not understand the adaptive significance of countershading
in rodents. Similarly, we understand the genetic underpinnings (ALX3) of striping in striped mice
species [15] but not its adaptive significance. Moreover, we have yet to make genetic modifica-
tions in known pigmentation/patterning genes and then test their effects on survival and repro-
duction in the wild. This is now within our grasp since we have the capability to manipulate
genomes of a diversity of species [79,80].

Second but conversely, we need to understand the molecular and developmental basis of phe-
notypes that have already been shown to be adaptive. We can already do this for melanin in
humans and some rodents in fire climax populations [81,82]. For example, the MC1RΔ24 allele
is associated with melanism in both gray squirrels and fox squirrels [20]. However, there are
other advantages of melanism for species living in shady or humid dark environments [83,84]
(Figure 1F) that could be explored genetically. We are still a long way from knowing the molecular
underpinnings of say aposematism or primate skin and hair color.

Third, we need to combine evolutionary and developmental approaches to understand conver-

gence. For instance, the repeated appearance of pigment patterns and color morphs is key to
evo-devo biology and we need to map developmental mechanisms underlying pelage coloration
onto a phylogenetic tree to confirm that these mechanisms are conserved across the mammalian
clade. And while we are getting a good handle on simple whole body changes in color from both
genetic/developmental and ecological standpoints, we do not know if the rules governing mech-
anisms and functions are congruent across species. Once we can marry these disciplines the
study of mammalian coloration will take a large step towards reaching maturity [85].

Acknowledgements
We thank Hopi Hoekstra and three reviewers for suggestions.

References
1. Kipling, R. (1902) Just So Stories for Little Children, Oxford
University Press
2. Morse III, H.C. (1978) Introduction. In Origins of Inbred Mice
(Morse, H.C., ed.), pp. 3–21, Academic Press
3. Castle, W.E. (1903) Mendel's law of heredity. Science 18,
396–406
4. Cuénot, L. (1904) Les recherches expérimentales sur
l’hérédité mendélienne. Rev. Gén. Sc. Pures Appl. 15,
303–310
5. Haldane, J.B.S. et al. (1915) Reduplication in mice (preliminary
communication). J. Genet. 5, 133–135
6. Little, C.C. (1917) Evidence of multiple factors in mice and rats.
Am. Nat. 51, 457–480
7. Jackson, I.J. (1988) A cDNA encoding tyrosinase-related protein
maps to the brown locus in mouse. Proc. Natl. Acad. Sci. U.S.A.
85, 4392–4396
8. Kwon, B.S. et al. (1989) Isolation, chromosomal mapping, and
expression of the mouse tyrosinase gene. J. Invest. Dermatol.
93, 589–594
9. Bennett, D.C. and Lamoreux, M.L. (2003) The color loci of mice–
a genetic century. Pigment Cell Res. 16, 333–344
10. Jackson, I.J. (1994) Molecular and developmental genetics of
mouse coat color. Annu. Rev. Genet. 28, 189–217
11. Barsh, G.S. (1996) The genetics of pigmentation: from fancy
genes to complex traits. Trends Genet. 12, 299–305
12. Kaelin, C.B. and Barsh, G.S. (2013) Genetics of pigmentation in
dogs and cats. Annu. Rev. Anim. Biosci. 1, 125–156
13. Baxter, L.L. et al. (2004) Spotlight on spotted mice: a review of
white spotting mouse mutants and associated human pigmen-
tation disorders. Pigment Cell Res. 17, 215–224
14. Manceau, M. et al. (2011) The developmental role of Agouti in
color pattern evolution. Science 331, 1062–1065
15. Mallarino, R. et al. (2016) Developmental mechanisms of stripe
patterns in rodents. Nature 539, 518–523
16. Kaelin, C.B. et al. (2012) Specifying and sustaining pigmenta-
tion patterns in domestic and wild cats. Science 337,
1536–1540
17. Imsland, F. et al. (2015) Regulatory mutations in TBX3 disrupt
asymmetric hair pigmentation that underlies Dun camouflage
color in horses. Nat. Genet. 48, 152–158
18. Anderson, T.M. et al. (2009) Molecular and evolutionary history
of melanism in North American gray wolves. Science 323,
1339–1343
19. Jones, M.R. et al. (2018) Adaptive introgression underlies poly-
morphic seasonal camouflage in snowshoe hares. Science 22,
1355–1358

364 Trends in Ecology & Evolution, April 2020, Vol. 35, No. 4
Trends in Ecology & Evolution
20. McRobie, H.R. et al. (2019) Multiple origins of melanism in two
species of North American tree squirrel (Sciurus). BMC Evol.
Biol. 19, 140
21. Caro, T. et al. (2018) Ecocorrelates of pelage coloration in pigs
and peccaries. J. Mammal. 99, 1093–1100
22. Caro, T. et al. (2012) Pelage coloration in pinnipeds: functional
considerations. Behav. Ecol. 23, 765–774
23. Zimova, M. et al. (2016) High fitness costs of climate change-
induced camouflage mismatch. Ecol. Lett. 19, 299–307
24. Domb, L.G. and Pagel, M. (2001) Sexual swellings advertise
female quality in wild baboons. Nature 410, 204
25. Dubuc, C. et al. (2014) Is male rhesus macaque red color orna-
mentation attractive to females? Behav. Ecol. Sociobiol. 68,
1215–1224
26. Gerald, M.S. (2001) Primate colour predicts social status and
aggressive outcome. Anim. Behav. 61, 559–566
27. Setchell, J.M. and Dixson, A.F. (2001) Changes in the secondary
sexual adornments of male mandrills (Mandrillus sphinx) are associ-
ated with gain and loss of alpha status. Horm. Behav. 39, 177–184
28. Changizi, M.A. et al. (2006) Bare skin, blood and the evolution of
primate colour vision. Biol. Lett. 2, 217–221
29. Darwin, C. (1872) The Expression of Emotions in Man and
Animals, John Murray
30. Jacobs, G.H. (2009) Evolution of colour vision in mammals.
Philos. Trans. R. Soc. B 364, 2957–2967
31. Osorio, D. and Vorobyev, M. (1996) Colour vision as an adapta-
tion to frugivory in primates. Proc. R. Soc. Lond. B 263,
593–599
32. Dominy, N.J. and Lucas, P.W. (2001) Ecological importance of
trichromatic vision to primates. Nature 410, 363
33. Melin, A.D. et al. (2017) Trichromacy increases fruit intake rates
of wild capuchins (Cebus capucinus imitator). Proc. Natl. Acad.
Sci. U. S. A. 114, 10402–10407
34. Hiramatsu, C. et al. (2008) Importance of achromatic contrast in
short-range fruit foraging of primates. PLoS ONE 3, e3356
35. Melin, A.D. et al. (2013) Food search through the eyes of a mon-
key: a functional substitution approach for assessing the ecology
of primate color vision. Vis. Res. 86, 87–96
36. Fernandez, A.A. and Morris, M.R. (2007) Sexual selection and
trichromatic color vision in primates: Statistical support for the
preexisting-bias hypothesis. Am. Nat. 170, 10–20
37. Kamilar, J.M. et al. (2013) Did trichromatic color vision and red
hair color coevolve in primates? Am. J. Primatol. 75, 740–751
38. Jacobs, G.H. (1996) Primate photopigments and primate color
vision. Proc. Natl. Acad. Sci. U. S. A. 93, 577–581
39. Surridge, A.K. and Mundy, N.I. (2002) Trans-specific evolution of
opsin alleles and the maintenance of trichromatic colour vision in
Callitrichine primates. Mol. Ecol. 11, 2157–2169
40. Jacobs, R.L. et al. (2017) Novel opsin gene variation in large-
bodied, diurnal lemurs. Biol. Lett. 13, 20170050
41. Melin, A.D. et al. (2017) Howler monkey foraging ecology sug-
gests convergent evolution of routine trichromacy as an adapta-
tion for folivory. Ecol. Evol. 7, 1421–1434
42. Hiramatsu, C. et al. (2017) Experimental evidence that primate
trichromacy is well suited for detecting primate social colour sig-
nals. Proc. R. Soc. B 284, 20162458
43. Sumner, F.B. (1921) Desert and lava-dwelling mice, and the problem
of protective coloration in mammals. J. Mammal. 2, 75–86
44. Hoekstra, H.E. and Nachman, M.W. (2003) Different genes un-
derlie adaptive melanism in different populations of rock pocket
mice. Mol. Ecol. 12, 1185–1194
45. Dice, L. (1947) Effectiveness of selection by owls of deermice
(Peromyscus maniculatus) which contrast with their back-
ground. Contr. Vert. Biol. Lab. Univ. Mich. 34
46. Vignieri, S.N. et al. (2010) The selective advantage of crypsis in
mice. Evolution 64, 2153–2158
47. Hoekstra, H.E. and Nachman, M.W. (2005) Coat color variation
in rock pocket mice (Chaetodipus intermedius): from genotype
to phenotype. In Mammalian Diversification: From Chromo-
somes to Phylogeography (A Celebration of the Career of
James L. Patton) (Lacey, E.I. and Myers, P., eds), pp. 79–99,
University of California Press, Berkeley
48. Boratyński, Z. et al. (2014) Large spatial scale of the phenotype-
environment color matching in two cryptic species of African de-
sert jerboas (Dipodidae: Jaculus). PLoS ONE 9, e94342
49. Stoner, C.J. et al. (2003) The adaptive significance of coat
colouration in lagomorphs. Biol. J. Linn. Soc. 79, 309–328
50. Allen, W.L. et al. (2010) Why the leopard got its spots: relating
pattern development to ecology in felids. Proc. R. Soc. Lond.
B 278, 1373–1380
51. Caro, T. et al. (2011) The functional significance of colouration in
cetaceans. Evol. Ecol. 25, 1231–1245
52. Ruxton, G.D. et al. (2018) Avoiding Attack: the Evolutionary
Ecology of Crypsis, Aposematism, and Mimicry, Oxford
University Press
53. Allen, W.L. et al. (2012) A quantitative test of the predicted rela-
tionship between countershading and lighting environment.
Am. Nat. 180, 762–776
54. Moreira, L.A.A. et al. (2019) Platyrrhine color signals: new hori-
zons to pursue. Evol. Anthropol. 28, 236–248
55. Caro, T. (2011) Black and white coloration in mammals: review
and synthesis. In Animal Camouflage: Mechanisms and Function
(Stevens, M. and Merilaita, S., eds), pp. 298–329, Cambridge
University Press
56. West, P.M. and Packer, C. (2002) Sexual selection, temperature,
and the lion's mane. Science 297, 1339–1343
57. Stankowich, T. et al. (2011) Bold coloration and the evolution of
aposematism in terrestrial carnivores. Evolution 65, 3090–3099
58. Caro, T. and Stankowich, T. (2009) The function of contrasting
pelage markings in artiodactyls. Behav. Ecol. 21, 78–84
59. Kamler, J.F. and Ballard, W.B. (2006) Ear flashing behavior of
black-tailed jackrabbits (Lepus californicus). Am. Midl. Nat.
155, 402–403
60. Santana, S.E. et al. (2012) Adaptive evolution of facial colour pat-
terns in Neotropical primates. Proc. R. Soc. Lond. B 279,
2204–2211
61. Allen, W.L. et al. (2014) Character displacement of
Cercopithecini primate visual signals. Nat. Commun. 5, 4266
62. Caro, T. and Allen, W. (2017) Interspecific visual signaling in an-
imals and plants: a functional classification. Philos. Trans. R.
Soc. B. 372, 20160344
63. Caro, T. (2009) Contrasting colouration in terrestrial mammals.
Philos. Trans. R. Soc. B. 364, 537–548
64. Caro, T. (2016) Zebra Stripes, University of Chicago Press
65. Caro, T. et al. (2019) Benefits of zebra stripes: behaviour of taba-
nid flies around zebras and horses. PLoS One 14, e0210831
66. Kojima, T. et al. (2019) Cows painted with zebra-like striping can
avoid biting fly attack. PLoS One 14, e0223447
67. Caro, T. et al. (2017) Why is the giant panda black and white?
Behav. Ecol. 28, 657–667
68. Delhey, K. (2017) Gloger’s rule. Curr. Biol. 27, R689–R691
69. Delhey, K. (2018) Darker where cold and wet: Australian birds fol-
low their own version of Gloger's rule. Ecography 41, 673–683
70. Hetem, R.S. et al. (2009) Body temperature, thermoregulatory
behaviour and pelt characteristics of three colour morphs of
springbok (Antidorcas marsupialis). Comp. Biochem. Physiol.
Part A: Mol. Integr. Physiol. 152, 379–388
71. Jablonski, N.G. and Chaplin, G. (2000) The evolution of human
skin coloration. J. Hum. Evol. 39, 57–106
72. Jablonski, N.G. and Chaplin, G. (2010) Human skin pigmentation
as an adaptation to UV radiation. Proc. Natl. Acad. Sci. U. S. A.
107, 8962–8968
73. Zimova, M. et al. (2018) Function and underlying mechanisms of
seasonal colour molting in mammals and birds: what keeps
them changing in a warming world? Biol. Rev. 93, 1478–1498
74. Hoekstra, H.E. (2006) Genetics, development and evolution of
adaptive pigmentation in vertebrates. Heredity 97, 222
75. Hubbard, J.K. et al. (2010) Vertebrate pigmentation: from
underlying genes to adaptive function. Trends Genet. 26,
231–239
76. Barrett, R.D.H. et al. (2019) Linking a mutation to survival in wild
mice. Science 363, 499–504
77. Hoekstra, H.E. et al. (2004) Ecological genetics of adaptive color
polymorphism in pocket mice: geographic variation in selected
and neutral genes. Evolution 58, 1329–1341
78. Linnen, C.R. et al. (2009) On the origin and spread of an adaptive
allele in deer mice. Science 325, 1095–1098
79. Niu, Y. et al. (2014) Generation of gene-modified Cynomolgus
monkey via Cas9/RNA-Mediated gene targeting in one-cell
embryos. Cell 156, 836–843
Trends in Ecology & Evolution, April 2020, Vol. 35, No. 4 365
Trends in Ecology & Evolution
80. Horie, K. et al. (2019) Oxytocin receptor knockout prairie voles
generated by CRISPR/Cas9 editing show reduced preference
for social novelty and exaggerated repetitive behaviors. Horm.
Behav. 111, 60–69
81. Kiltie, R.A. (1989) Wildfire and the evolution of dorsal melanism in
fox squirrels, Sciurus niger. J. Mammal. 70, 726–739
82. McRobie, H. et al. (2009) The genetic basis of melanism in the
gray squirrel (Sciurus carolinensis). J. Hered. 100, 709–714
366 Trends in Ecology & Evolution, April 2020, Vol. 35, No. 4
83. Kawanishi, K. et al. (2010) Near fixation of melanism in
leopards of the Malay Peninsula. J. Zool. 282,
201–206
84. Nigenda-Morales, S.F. et al. (2018) Transcriptomic analysis of
skin pigmentation in the Virginia opossum (Didelphis virginiana).
Mol. Ecol. 2018, 1–15
85. Cuthill, I.C. et al. (2017) The biology of color. Science 357,
eaan0221